Advertisement

Cell and Tissue Research

, Volume 371, Issue 2, pp 223–236 | Cite as

Laminin-derived Ile-Lys-Val-ala-Val: a promising bioactive peptide in neural tissue engineering in traumatic brain injury

  • Sajad Sahab Negah
  • Alireza Khooei
  • Fariborz Samini
  • Ali Gorji
Review

Abstract

The adult brain has a very limited regeneration capacity and there is no effective treatment currently available for brain injury. Neuroprotective drugs aim to reduce the intensity of cell degeneration but do not trigger tissue regeneration. Cell replacement therapy is a novel strategy to overcome brain injury-induced disability. To enhance cell viability and neuronal differentiation, developing bioactive scaffolds combined with stem cells for transplantation is a crucial approach in brain tissue engineering. Cell interactions with the extracellular matrix (ECM) play a vital role in neuronal cell survival, neurite outgrowth, attachment, migration, differentiation, and proliferation. Thus, appropriate cell–ECM interactions are essential when designing and modifying scaffolds for application in neural tissue engineering. To improve cell–ECM interactions, scaffolds can be modified with bioactive peptides. Here, we discuss the characteristic features of laminin-derived Ile-Lys-Val-Ala-Val (IKVAV) sequence as a bio-functional motif in scaffolds and the behavior of stem cells in scaffolds conjugated with the IKVAV peptide. The incorporation of this bioactive peptide in nanofiber scaffolds markedly improves stem cell behavior and may be a potential method for cell replacement therapy in traumatic brain injury.

Keywords

IKVAV peptide Cell therapy Brain injury Tissue engineering Stem cells 

Abbreviations

2D

Two-dimensional

3D

Three-dimensional

APP

Beta-amyloid precursor protein

BMMSCs

Bone marrow mesenchymal stem cell

CNS

Central nervous system

CSPGs

Chondroitin sulfate proteoglycans

DRG

Dorsal root ganglion

ECM

Extracellular matrix

ESCs

Embryonic stem cells

GaN

Gallium nitride

hNSCs

Human neural stem cells

hUC-MSCs

Human umbilical cord mesenchymal stem cells

IKVAV

Ile-Lys-Val-Ala-Val

ILK

Integrin-linked kinase

iNSCs

Induced neural stem cells

LBP110

Laminin-binding protein

MAPK/ERK1/2

Mitogen-activated protein kinase/extracellular signal-regulated kinase

NSCs

Neural stem cells

OPCs

Oligodendrocyte progenitor cells

P(HEMA-AEMA)

2-hydroxyethyl methacrylate with 2-aminoethyl methacrylate

PEG

Polyethylene glycol

PI3K/Ak

Phosphatidylinositol 3-kinase/protein kinase B

PLEOF

Lactide-co-ethylene oxide-co-fumarate

RGD

Arg-Gly-Asp

R-GSIK

RADA4GGSIKVAV

SAP

Self-assembling peptide

SAPNS

Self-assembly peptide nanofiber scaffold

SCZ

Subcallosal zone

SGZ

Subgranular zone

SIKVAV

Ac-CGGASIKVAVS-OH

TBI

Traumatic brain injury

VZ-SVZ

Ventricular–subventricular zone

YIGSR

Tyr-Ile-Gly-Ser-Arg

Notes

Acknowledgement

This study was supported by the Iran National Science Foundation (INSF) to AG.

Compliance with ethical standards

Conflict of interest

There is no conflict of interest.

References

  1. Aligholi H, Hassanzadeh G, Azari H, Rezayat SM, Mehr SE, Akbari M, Attari F, Khaksarian M, Gorji A (2014) A new and safe method for stereotactically harvesting neural stem/progenitor cells from the adult rat subventricular zone. J Neurosci Methods 30 225:81–89CrossRefGoogle Scholar
  2. Aligholi H, Rezayat SM, Azari H, Ejtemaei Mehr S, Akbari M, Modarres Mousavi SM, Attari F, Alipour F, Hassanzadeh G, Gorji A (2016) Preparing neural stem/progenitor cells in PuraMatrix hydrogel for transplantation after brain injury in rats: a comparative methodological study. Brain Res 1642:197–208PubMedCrossRefGoogle Scholar
  3. Bakshi A, Keck CA, Koshkin VS, LeBold DG, Siman R, Snyder EY, McIntosh TK (2005) Caspase-mediated cell death predominates following engraftment of neural progenitor cells into traumatically injured rat brain. Brain Res 1065:8–19PubMedCrossRefGoogle Scholar
  4. Bandtlow CE, Zimmermann DR (2000) Proteoglycans in the developing brain: new conceptual insights for old proteins. Physiol Rev 80:1267–1290PubMedCrossRefGoogle Scholar
  5. Barros CS, Franco SJ, Müller U (2011) Extracellular matrix: functions in the nervous system. Cold Spring Harb Perspect Biol 3:a005108PubMedPubMedCentralCrossRefGoogle Scholar
  6. Bokhari MA, Akay G, Zhang S, Birch MA (2005) The enhancement of osteoblast growth and differentiation in vitro on a peptide hydrogel—polyHIPE polymer hybrid material. Biomaterials 26:5198–5208PubMedCrossRefGoogle Scholar
  7. Bonneh-Barkay D, Wiley CA (2009) Brain extracellular matrix in neurodegeneration. Brain Pathol 19:573–585PubMedCrossRefGoogle Scholar
  8. Brizzi MF, Tarone G, Defilippi P (2012) Extracellular matrix, integrins, and growth factors as tailors of the stem cell niche. Curr Opin Cell Biol 24:645–651PubMedCrossRefGoogle Scholar
  9. Carone TW, Hasenwinkel JM (2006) Mechanical and morphological characterization of homogeneous and bilayered poly (2-hydroxyethyl methacrylate) scaffolds for use in CNS nerve regeneration. J Biomed Mater Res B 78:274–282CrossRefGoogle Scholar
  10. Cheng T-Y, Chen M-H, Chang W-H, Huang M-Y, Wang T-W (2013) Neural stem cells encapsulated in a functionalized self-assembling peptide hydrogel for brain tissue engineering. Biomaterials 34:2005–2016PubMedCrossRefGoogle Scholar
  11. Chiu C-C, Liao Y-E, Yang L-Y, Wang J-Y, Tweedie D, Karnati HK, Greig NH, Wang J-Y (2016) Neuroinflammation in animal models of traumatic brain injury. J Neurosci Methods 272:38–49PubMedPubMedCentralCrossRefGoogle Scholar
  12. Clark RA (2008) Synergistic signaling from extracellular matrix–growth factor complexes. J Investig Dermatol 128:1354–1355PubMedCrossRefGoogle Scholar
  13. Cooke M, Vulic K, Shoichet M (2010) Design of biomaterials to enhance stem cell survival when transplanted into the damaged central nervous system. Soft Matter 6:4988–4998CrossRefGoogle Scholar
  14. Dehsorkhi A, Gouveia RM, Smith AM, Hamley IW, Castelletto V, Connon CJ, Reza M, Ruokolainen J (2015) Self-assembly of a dual functional bioactive peptide amphiphile incorporating both matrix metalloprotease substrate and cell adhesion motifs. Soft Matter 11:3115–3124PubMedCrossRefGoogle Scholar
  15. Doering LC (2010) Protocols for neural cell culture. Springer, New YorkGoogle Scholar
  16. Drury JL, Mooney DJ (2003) Hydrogels for tissue engineering: scaffold design variables and applications. Biomaterials 24:4337–4351PubMedCrossRefGoogle Scholar
  17. Einstein O, Ben-Menachem-Tzidon O, Mizrachi-Kol R, Reinhartz E, Grigoriadis N, Ben-Hur T (2006) Survival of neural precursor cells in growth factor-poor environment: implications for transplantation in chronic disease. Glia 53:449–455PubMedCrossRefGoogle Scholar
  18. El-Sherbiny IM, Yacoub MH (2013) Hydrogel scaffolds for tissue engineering: progress and challenges. Glob Cardiol Sci Pract 38Google Scholar
  19. Faissner A, Pyka M, Geissler M, Sobik T, Frischknecht R, Gundelfinger ED, Seidenbecher C (2010) Contributions of astrocytes to synapse formation and maturation—potential functions of the perisynaptic extracellular matrix. Brain Res Rev 63:26–38PubMedCrossRefGoogle Scholar
  20. Francis NL, Bennett NK, Halikere A, Pang ZP, Moghe PV (2016) Self-assembling peptide Nanofiber scaffolds for 3-D reprogramming and transplantation of human pluripotent stem cell-derived neurons. ACS Biomater Sci Eng 2:1030–1038Google Scholar
  21. Francisco AT, Mancino RJ, Bowles RD, Brunger JM, Tainter DM, Chen Y-T, Richardson WJ, Guilak F, Setton LA (2013) Injectable laminin-functionalized hydrogel for nucleus pulposus regeneration. Biomaterials 34:7381–7388PubMedPubMedCentralCrossRefGoogle Scholar
  22. Frick C, Muller M, Wank U, Tropitzsch A, Kramer B, Senn P, Rask-Andersen H, Wiesmuller KH, Lowenheim H (2016) Biofunctionalized peptide-based hydrogels provide permissive scaffolds to attract neurite outgrowth from spiral ganglion neurons. Colloids Surf B 149:105–114CrossRefGoogle Scholar
  23. Frith JE, Menzies DJ, Cameron AR, Ghosh P, Whitehead DL, Gronthos S, Zannettino AC, Cooper-White JJ (2014) Effects of bound versus soluble pentosan polysulphate in PEG/HA-based hydrogels tailored for intervertebral disc regeneration. Biomaterials 35:1150–1162PubMedCrossRefGoogle Scholar
  24. Fukunaga K, Tsutsumi H, Mihara H (2015) Cell differentiation on disk-and string-shaped hydrogels fabricated from Ca2+−responsive self-assembling peptides. Biopolymers 106:476–483Google Scholar
  25. Galvez-Contreras AY, Quiñones-Hinojosa A, Gonzalez-Perez O (2013) The role of EGFR and ErbB family related proteins in the oligodendrocyte specification in germinal niches of the adult mammalian brain. Front Cell Neurosci 7:258PubMedPubMedCentralCrossRefGoogle Scholar
  26. Gardner RC, Burke JF, Nettiksimmons J, Goldman S, Tanner CM, Yaffe K (2015) Traumatic brain injury in later life increases risk for Parkinson disease. Ann Neurol 77:987–995PubMedPubMedCentralCrossRefGoogle Scholar
  27. Gardner RC, Burke JF, Nettiksimmons J, Kaup A, Barnes DE, Yaffe K (2014) Dementia risk after traumatic brain injury vs nonbrain trauma: the role of age and severity. JAMA Neurol 71:1490–1497PubMedPubMedCentralCrossRefGoogle Scholar
  28. Gardner RC, Yaffe K (2015) Epidemiology of mild traumatic brain injury and neurodegenerative disease. Mol Cell Neurosci 66:75–80PubMedPubMedCentralCrossRefGoogle Scholar
  29. Gelain F, Bottai D, Vescovi A, Zhang S (2006) Designer self-assembling peptide nanofiber scaffolds for adult mouse neural stem cell 3-dimensional cultures. PLoS ONE 1:e119PubMedPubMedCentralCrossRefGoogle Scholar
  30. Ghasemi-Mobarakeh L, Prabhakaran MP, Morshed M, Nasr-Esfahani M-H, Ramakrishna S (2008) Electrospun poly (ɛ-caprolactone)/gelatin nanofibrous scaffolds for nerve tissue engineering. Biomaterials 29:4532–4539PubMedCrossRefGoogle Scholar
  31. Goldstein LE, Fisher AM, Tagge CA, Zhang X-L, Velisek L, Sullivan JA, Upreti C, Kracht JM, Ericsson M, Wojnarowicz MW (2012) Chronic traumatic encephalopathy in blast-exposed military veterans and a blast neurotrauma mouse model. Sci Translat Med 4:134ra160–134ra160Google Scholar
  32. Graf J, Iwamoto Y, Sasaki M, Martin GR, Kleinman HK, Robey FA, Yamada Y (1987) Identification of an amino acid sequence in laminin mediating cell attachment, chemotaxis, and receptor binding. Cell 48:989–996PubMedCrossRefGoogle Scholar
  33. Greig NH, Tweedie D, Rachmany L, Li Y, Rubovitch V, Schreiber S, Chiang Y-H, Hoffer BJ, Miller J, Lahiri DK (2014) Incretin mimetics as pharmacologic tools to elucidate and as a new drug strategy to treat traumatic brain injury. Alzheimers Dement 10:S62–S75PubMedPubMedCentralCrossRefGoogle Scholar
  34. Hall D, Reichardt L, Crowley E, Holley B, Moezzi H, Sonnenberg A, Damsky C (1990) The alpha 1/beta 1 and alpha 6/beta 1 integrin heterodimers mediate cell attachment to distinct sites on laminin. J Cell Biol 110:2175–2184PubMedCrossRefGoogle Scholar
  35. Han DW, Greber B, Wu G, Tapia N, Araúzo-Bravo MJ, Ko K, Bernemann C, Stehling M, Schöler HR (2011) Direct reprogramming of fibroblasts into epiblast stem cells. Nat Cell Biol 13:66–71PubMedCrossRefGoogle Scholar
  36. Han DW, Tapia N, Hermann A, Hemmer K, Höing S, Araúzo-Bravo MJ, Zaehres H, Wu G, Frank S, Moritz S (2012) Direct reprogramming of fibroblasts into neural stem cells by defined factors. Cell Stem Cell 10:465–472PubMedCrossRefGoogle Scholar
  37. Han R, Tu LY, Yang MK, Xu T, Ma Y, Bi XJ, Sheng WB (2013) Combined application of neural stem cell and self-assembly isoleucine-lysine-valine-alanine-valine nanofiber gel transplantation in the promotion of function recovery of spinal cord injury in rats. Zhonghua Yi Xue Za Zhi 93:1669–1673PubMedGoogle Scholar
  38. Harting MT, Baumgartner JE, Worth LL, Ewing-Cobbs L, Gee AP, Day M-C, Cox CS Jr (2008) Cell therapies for traumatic brain injury. Neurosurg Focus 24:E18PubMedPubMedCentralCrossRefGoogle Scholar
  39. Harting MT, Jimenez F, Xue H, Fischer UM, Baumgartner J, Dash PK, Cox CS Jr (2009a) Intravenous mesenchymal stem cell therapy for traumatic brain injury: laboratory investigation. J Neurosurg 110:1189–1197PubMedPubMedCentralCrossRefGoogle Scholar
  40. Harting MT, Sloan LE, Jimenez F, Baumgartner J, Cox CS (2009b) Subacute neural stem cell therapy for traumatic brain injury. J Surg Res 153:188–194PubMedCrossRefGoogle Scholar
  41. Hoffman K, Skrtic D, Sun J, Tutak W (2014) Airbrushed composite polymer Zr-ACP nanofiber scaffolds with improved cell penetration for bone tissue regeneration. Tissue Eng Part C 21:284–291CrossRefGoogle Scholar
  42. Holmes TC, de Lacalle S, Su X, Liu G, Rich A, Zhang S (2000) Extensive neurite outgrowth and active synapse formation on self-assembling peptide scaffolds. Proc Natl Acad Sci U S A 97:6728–6733PubMedPubMedCentralCrossRefGoogle Scholar
  43. Horgan CC, Rodriguez AL, Li R, Bruggeman KF, Stupka N, Raynes JK, Day L, White JW, Williams RJ, Nisbet DR (2016) Characterisation of minimalist co-assembled fluorenylmethyloxycarbonyl self-assembling peptide systems for presentation of multiple bioactive peptides. Acta Biomater 38:11–22PubMedCrossRefGoogle Scholar
  44. Horner PJ, Gage FH (2000) Regenerating the damaged central nervous system. Nature 407:963–970PubMedCrossRefGoogle Scholar
  45. Hosseinkhani H, Hiraoka Y, Li C-H, Chen Y-R, Yu D-S, Hong P-D, Ou K-L (2013) Engineering three-dimensional collagen-IKVAV matrix to mimic neural microenvironment. ACS Chem Neurosci 4:1229–1235PubMedPubMedCentralCrossRefGoogle Scholar
  46. Hou S, Lu P (2016) Direct reprogramming of somatic cells into neural stem cells or neurons for neurological disorders. Neural Regen Res 11:28PubMedPubMedCentralCrossRefGoogle Scholar
  47. Hynd MR, Turner JN, Shain W (2007) Applications of hydrogels for neural cell engineering. J Biomater Sci Polym Ed 18:1223–1244PubMedCrossRefGoogle Scholar
  48. Ieda M, Fu J-D, Delgado-Olguin P, Vedantham V, Hayashi Y, Bruneau BG, Srivastava D (2010) Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell 142:375–386PubMedPubMedCentralCrossRefGoogle Scholar
  49. Jewett SA, Makowski MS, Andrews B, Manfra MJ, Ivanisevic A (2012) Gallium nitride is biocompatible and non-toxic before and after functionalization with peptides. Acta Biomater 8:728–733PubMedCrossRefGoogle Scholar
  50. Kam L, Shain W, Turner J, Bizios R (2001) Axonal outgrowth of hippocampal neurons on micro-scale networks of polylysine-conjugated laminin. Biomaterials 22:1049–1054PubMedCrossRefGoogle Scholar
  51. Kazemi S, Baltzer W, Mansouri H, Schilke K, Mata J (2016) IKVAV-containing cell membrane penetrating peptide treatment induces changes in cellular morphology after spinal cord injury. Mod Appl Sci 10:149CrossRefGoogle Scholar
  52. Khoshakhlagh P, Moore MJ (2015) Photoreactive interpenetrating network of hyaluronic acid and Puramatrix as a selectively tunable scaffold for neurite growth. Acta Biomater 16:23–34PubMedCrossRefGoogle Scholar
  53. Kibbey M, Johnson B, Petryshyn R, Jucker M, Kleinman H (1995) A 110-kD nuclear shuttling protein, nucleolin, binds to the neurite-promoting IKVAV site of laminin-1. J Neurosci Res 42:314–322PubMedCrossRefGoogle Scholar
  54. Kibbey MC, Jucker M, Weeks BS, Neve RL, Van Nostrand WE, Kleinman HK (1993) Beta-Amyloid precursor protein binds to the neurite-promoting IKVAV site of laminin. Proc Natl Acad Sci U S A 90:10150–10153PubMedPubMedCentralCrossRefGoogle Scholar
  55. Kim SM, Flaßkamp H, Hermann A, Araúzo-Bravo MJ, Lee SC, Lee SH, Seo EH, Lee SH, Storch A, Lee HT (2014) Direct conversion of mouse fibroblasts into induced neural stem cells. Nat Protoc 9:871–881PubMedCrossRefGoogle Scholar
  56. Kim SU, De Vellis J (2009) Stem cell-based cell therapy in neurological diseases: a review. J Neurosci Res 87:2183–2200PubMedCrossRefGoogle Scholar
  57. Kleinman HK, Weeks BS, Cannon FB, Sweeney TM, Sephel GC, Clement B, Zain M, Olson MO, Jucker M, Burrous BA (1991) Identification of a 110-kDa nonintegrin cell surface laminin-binding protein which recognizes an a chain neurite-promoting peptide. Arch Biochem Biophys 290:320–325PubMedCrossRefGoogle Scholar
  58. Koss K, Churchward M, Nguyen A, Yager J, Todd K, Unsworth L (2016) Brain biocompatibility and microglia response towards engineered self-assembling (RADA) 4 nanoscaffolds. Acta Biomater 35:127–137PubMedCrossRefGoogle Scholar
  59. Koss K, Unsworth L (2016) Neural tissue engineering: bioresponsive nanoscaffolds using engineered self-assembling peptides. Acta Biomater 44:2–15PubMedCrossRefGoogle Scholar
  60. Koutsopoulos S (2016) Self-assembling peptide nanofiber hydrogels in tissue engineering and regenerative medicine: progress, design guidelines, and applications. J Biomed Mater Res A 104:1002–1016PubMedCrossRefGoogle Scholar
  61. Lau LW, Cua R, Keough MB, Haylock-Jacobs S, Yong VW (2013) Pathophysiology of the brain extracellular matrix: a new target for remyelination. Nat Rev Neurosci 14:722–729PubMedCrossRefGoogle Scholar
  62. Li B, Qiu T, Zhang P, Wang X, Yin Y, Li S (2014) IKVAV regulates ERK1/2 and Akt signalling pathways in BMMSC population growth and proliferation. Cell Prolif 47:133–145PubMedPubMedCentralCrossRefGoogle Scholar
  63. Li Q, Cheung WH, Chow KL, Ellis-Behnke RG, Chau Y (2012) Factorial analysis of adaptable properties of self-assembling peptide matrix on cellular proliferation and neuronal differentiation of pluripotent embryonic carcinoma. Nanomedicine 8:748–756PubMedCrossRefGoogle Scholar
  64. Li X, Katsanevakis E, Liu X, Zhang N, Wen X (2012) Engineering neural stem cell fates with hydrogel design for central nervous system regeneration. Prog Polym Sci 37:1105–1129CrossRefGoogle Scholar
  65. Li X, Liu X, Josey B, Chou CJ, Tan Y, Zhang N, Wen X (2014) Short laminin peptide for improved neural stem cell growth. Stem Cells Transl Med 3:662–670PubMedPubMedCentralCrossRefGoogle Scholar
  66. Liesi P, Närvänen A, Soos J, Sariola H, Snounou G (1989) Identification of a neurite outgrowth-promoting domain of laminin using synthetic peptides. FEBS Lett 244:141–148PubMedCrossRefGoogle Scholar
  67. Lin X, Takahashi K, Liu Y, Zamora P (2006) Enhancement of cell attachment and tissue integration by a IKVAV containing multi-domain peptide. Biochim Biophys Acta 1760:1403–1410PubMedCrossRefGoogle Scholar
  68. Liu X, Pi B, Wang H, Wang X-M (2015) Self-assembling peptide nanofiber hydrogels for central nervous system regeneration. Front Mater Sci 9:1–13CrossRefGoogle Scholar
  69. Lu T, Li Y, Chen T (2013) Techniques for fabrication and construction of three-dimensional scaffolds for tissue engineering. Int J Nanomed 8:337–350CrossRefGoogle Scholar
  70. Luo Z, Zhang S (2012) Designer nanomaterials using chiral self-assembling peptide systems and their emerging benefit for society. Chem Soc Rev 41:4736–4754PubMedCrossRefGoogle Scholar
  71. Ma PX, Zhang R (1999) Synthetic nano-scale fibrous extracellular matrix. J Biomed Mater Res 46(1):60–72PubMedCrossRefGoogle Scholar
  72. Macková H, Plichta Z, Proks V, Kotelnikov I, Kučka J, Hlídková H, Horák D, Kubinová Š, Jiráková K (2016) RGDS-and SIKVAVS-modified Superporous poly (2-hydroxyethyl methacrylate) scaffolds for tissue engineering applications. Macromol Biosci 16:1621–1631PubMedCrossRefGoogle Scholar
  73. Mammadov R, Mammadov B, Toksoz S, Aydin B, Yagci R, Tekinay AB, Guler MO (2011) Heparin mimetic peptide nanofibers promote angiogenesis. Biomacromolecules 12:3508–3519PubMedCrossRefGoogle Scholar
  74. Martínez-Morales P, Revilla A, Ocana I, Gonzalez C, Sainz P, McGuire D, Liste I (2013) Progress in stem cell therapy for major human neurological disorders. Stem Cell Rev Rep 9:685–699CrossRefGoogle Scholar
  75. Martino MM, Briquez PS, Ranga A, Lutolf MP, Hubbell JA (2013) Heparin-binding domain of fibrin (ogen) binds growth factors and promotes tissue repair when incorporated within a synthetic matrix. Proc Natl Acad Sci U S A 110:4563–4568PubMedPubMedCentralCrossRefGoogle Scholar
  76. Maturavongsadit P, Bi X, Gado TA, Nie Y-Z, Wang Q (2016) Adhesive peptides conjugated PAMAM dendrimer as a coating polymeric material enhancing cell responses. Chin Chem Lett (in press)Google Scholar
  77. Monteiro N, Ribeiro D, Martins A, Faria S, Fonseca NA, Moreira JN, Reis RL, Neves NM (2014) Instructive nanofibrous scaffold comprising runt-related transcription factor 2 gene delivery for bone tissue engineering. ACS Nano 8:8082–8094PubMedCrossRefGoogle Scholar
  78. Nakaji-Hirabayashi T, Kato K, Iwata H (2013) In vivo study on the survival of neural stem cells transplanted into the rat brain with a collagen hydrogel that incorporates laminin-derived polypeptides. Bioconjug Chem 24:1798–1804PubMedCrossRefGoogle Scholar
  79. Negah SS, Khaksar Z, Aligholi H, Sadeghi SM, Mousavi SMM, Kazemi H, Jahan-Abad AJ, Gorji A (2016) Enhancement of neural stem cell survival, proliferation, migration, and differentiation in a novel self-assembly peptide Nanofibber scaffold. Mol Neurobiol:1–13Google Scholar
  80. Nisbet DR, Rodda AE, Horne MK, Forsythe JS, Finkelstein DI (2010) Implantation of functionalized thermally gelling xyloglucan hydrogel within the brain: associated neurite infiltration and inflammatory response. Tissue Eng A 16:2833–2842CrossRefGoogle Scholar
  81. Nisbet DR, Williams RJ (2012) Self-assembled peptides: characterisation and in vivo response. Biointerphases 7:2PubMedCrossRefGoogle Scholar
  82. Nomizu M, Weeks BS, Weston CA, Kim WH, Kleinman HK, Yamada Y (1995) Structure-activity study of a laminin α1 chain active peptide segment Ile-Lys-Val-ala-Val (IKVAV). FEBS Lett 365:227–231PubMedCrossRefGoogle Scholar
  83. Palmgren B, Jiao Y, Novozhilova E, Stupp SI, Olivius P (2012) Survival, migration and differentiation of mouse tau-GFP embryonic stem cells transplanted into the rat auditory nerve. Exp Neurol 235:599–609PubMedCrossRefGoogle Scholar
  84. Pan L, North HA, Sahni V, Jeong SJ, Mcguire TL, Berns EJ, Stupp SI, Kessler JA (2014) β1-Integrin and integrin linked kinase regulate astrocytic differentiation of neural stem cells. PLoS ONE 9:e104335PubMedPubMedCentralCrossRefGoogle Scholar
  85. Pêgo AP, Kubinova S, Cizkova D, Vanicky I, Mar FM, Sousa MM, Sykova E (2012) Regenerative medicine for the treatment of spinal cord injury: more than just promises? J Cell Mol Med 16:2564–2582PubMedPubMedCentralCrossRefGoogle Scholar
  86. Peppas NA, Keys KB, Torres-Lugo M, Lowman AM (1999) Poly (ethylene glycol)-containing hydrogels in drug delivery. J Control Release 62:81–87PubMedCrossRefGoogle Scholar
  87. Pettikiriarachchi JT, Parish CL, Shoichet MS, Forsythe JS, Nisbet DR (2010) Biomaterials for brain tissue engineering. Aust J Chem 63:1143–1154CrossRefGoogle Scholar
  88. Powell SK, Rao J, Roque E, Nomizu M, Kuratomi Y, Yamada Y, Kleinman HK (2000) Neural cell response to multiple novel sites on laminin-1. J Neurosci Res 61:302–312PubMedCrossRefGoogle Scholar
  89. Raeber G, Lutolf M, Hubbell J (2005) Molecularly engineered PEG hydrogels: a novel model system for proteolytically mediated cell migration. Biophys J 89:1374–1388PubMedPubMedCentralCrossRefGoogle Scholar
  90. Raspa A, Pugliese R, Maleki M, Gelain F (2016) Recent therapeutic approaches for spinal cord injury. Biotechnol Bioeng 113:253–259PubMedCrossRefGoogle Scholar
  91. Robel S, Mori T, Zoubaa S, Schlegel J, Sirko S, Faissner A, Goebbels S, Dimou L, Götz M (2009) Conditional deletion of β1-integrin in astroglia causes partial reactive gliosis. Glia 57:1630–1647PubMedCrossRefGoogle Scholar
  92. Roll L, Faissner A (2014) Influence of the extracellular matrix on endogenous and transplanted stem cells after brain damage. Front Cell Neurosci 8:219PubMedPubMedCentralCrossRefGoogle Scholar
  93. Negah SS, Aligholi H, Khaksar Z, Kazemi H, Modarres Mousavi SM, Safahani M, Barati Dowom P, Gorji A (2016) Survival, proliferation, and migration of human meningioma stem-like cells in a nanopeptide scaffold. Iran J Basic Med Sci 19:1271–1278Google Scholar
  94. Sang LY-H, Liang Y-X, Li Y, Wong W-M, Tay DK-C, So K-F, Ellis-Behnke RG, Wu W, Cheung RT-F (2015) A self-assembling nanomaterial reduces acute brain injury and enhances functional recovery in a rat model of intracerebral hemorrhage. Nanomedicine 11:611–620PubMedCrossRefGoogle Scholar
  95. Schense JC, Hubbell JA (2000) Three-dimensional migration of neurites is mediated by adhesion site density and affinity. J Biol Chem 275:6813–6818PubMedCrossRefGoogle Scholar
  96. Semino CE, Merok JR, Crane GG, Panagiotakos G, Zhang S (2003) Functional differentiation of hepatocyte-like spheroid structures from putative liver progenitor cells in three-dimensional peptide scaffolds. Differentiation 71:262–270PubMedCrossRefGoogle Scholar
  97. Sephel G, Tashiro K, Sasaki M, Greatorex D, Martin G, Yamada Y, Kleinman H (1989) Laminin a chain synthetic peptide which supports neurite outgrowth. Biochem Biophys Res Commun 162:821–829PubMedCrossRefGoogle Scholar
  98. Shi W, Huang C, Xu X, Jin G, Huang R, Huang J, Chen Y, Ju S, Wang Y, Shi Y (2016) Transplantation of RADA16-BDNF peptide scaffold with human umbilical cord mesenchymal stem cells forced with CXCR4 and activated astrocytes for repair of traumatic brain injury. Acta Biomater 45:247–261PubMedCrossRefGoogle Scholar
  99. Silva GA, Czeisler C, Niece KL, Beniash E, Harrington DA, Kessler JA, Stupp SI (2004) Selective differentiation of neural progenitor cells by high-epitope density nanofibers. Science 303:1352–1355PubMedCrossRefGoogle Scholar
  100. Soleman S, Filippov M, Dityatev A, Fawcett J (2013) Targeting the neural extracellular matrix in neurological disorders. Neuroscience 253:194–213PubMedCrossRefGoogle Scholar
  101. Song Y, Li Y, Zheng Q, Wu K, Guo X, Wu Y, Yin M, Wu Q, Fu X (2011) Neural progenitor cells survival and neuronal differentiation in peptide-based hydrogels. J Biomater Sci Polym Ed 22:475–487PubMedCrossRefGoogle Scholar
  102. Sun W, Incitti T, Migliaresi C, Quattrone A, Casarosa S, Motta A (2017) Viability and neuronal differentiation of neural stem cells encapsulated in silk fibroin hydrogel functionalized with an IKVAV peptide. J Tissue Eng Regen Med 11:1532–1541Google Scholar
  103. Sun Y, Li W, Wu X, Zhang N, Zhang Y, Ouyang S, Song X, Fang X, Seeram R, Xue W (2016) Functional self-assembling peptide nanofiber hydrogels designed for nerve degeneration. ACS Appl Mater Interfaces 8:2348–2359PubMedCrossRefGoogle Scholar
  104. Suri S, c CE (2010) Cell-laden hydrogel constructs of hyaluronic acid, collagen, and laminin for neural tissue engineering. Tissue Eng A 16:1703–1716Google Scholar
  105. Tavakol S, Saber R, Hoveizi E, Tavakol B, Aligholi H, Ai J, Rezayat SM (2016) Self-Assembling peptide nanofiber containing long motif of laminin induces neural differentiation, tubulin polymerization, and neurogenesis: In vitro, ex vivo, and in vivo studies. Mol Neurobiol 53 (8):5288–5299PubMedCrossRefGoogle Scholar
  106. Tajiri N, Duncan K, Antoine A, Pabon M, Acosta SA, de la Pena I, Hernadez-Ontiveros DG, Shinozuka K, Ishikawa H, Kaneko Y (2014) Stem cell-paved biobridge facilitates neural repair in traumatic brain injury. Front Syst Neurosci 8:116PubMedPubMedCentralCrossRefGoogle Scholar
  107. Tashiro K-I, Sephel GC, Weeks B, Sasaki M, Martin G, Kleinman HK, Yamada Y (1989) A synthetic peptide containing the IKVAV sequence from the a chain of laminin mediates cell attachment, migration, and neurite outgrowth. J Biol Chem 264:16174–16182PubMedGoogle Scholar
  108. Tate CC (2006) The role of extracellular matrix proteins in traumatic brain injury and cell transplantation. Dissertation, Georgia Institute of Technology, Emory UniversityGoogle Scholar
  109. Tsai EC, Dalton PD, Shoichet MS, Tator CH (2004) Synthetic hydrogel guidance channels facilitate regeneration of adult rat brainstem motor axons after complete spinal cord transection. J Neurotrauma 21:789–804PubMedCrossRefGoogle Scholar
  110. Tutak W, Sarkar S, Lin-Gibson S, Farooque TM, Jyotsnendu G, Wang D, Kohn J, Bolikal D, Simon CG Jr (2013) The support of bone marrow stromal cell differentiation by airbrushed nanofiber scaffolds. Biomaterials 34:2389–2398PubMedCrossRefGoogle Scholar
  111. Tweedie D, Rachmany L, Rubovitch V, Lehrmann E, Zhang Y, Becker KG, Perez E, Miller J, Hoffer BJ, Greig NH (2013) Exendin-4, a glucagon-like peptide-1 receptor agonist prevents mTBI-induced changes in hippocampus gene expression and memory deficits in mice. Exp Neurol 239:170–182PubMedCrossRefGoogle Scholar
  112. Tysseling-Mattiace VM, Sahni V, Niece KL, Birch D, Czeisler C, Fehlings MG, Stupp SI, Kessler JA (2008) Self-assembling nanofibers inhibit glial scar formation and promote axon elongation after spinal cord injury. J Neurosci 28:3814–3823PubMedPubMedCentralCrossRefGoogle Scholar
  113. Tzu J, Marinkovich MP (2008) Bridging structure with function: structural, regulatory, and developmental role of laminins. Int J Biochem Cell Biol 40:199–214PubMedCrossRefGoogle Scholar
  114. Vasita R, Katti DS (2006) Nanofibers and their applications in tissue engineering. Int J Nanomedicine 1(1):15–30PubMedPubMedCentralCrossRefGoogle Scholar
  115. Wei Y, Tian W, Yu X, Cui F, Hou S, Xu Q, Lee I-S (2007) Hyaluronic acid hydrogels with IKVAV peptides for tissue repair and axonal regeneration in an injured rat brain. Biomed Mater 2:S142PubMedCrossRefGoogle Scholar
  116. Wu B, Zheng Q, Wu Y, Guo X, Zou Z (2010) Effect of IKVAV peptide nanofiber on proliferation, adhesion and differentiation into neurocytes of bone marrow stromal cells. J Huazhong Univ Sci Technol [Med Sci] 30:178–182CrossRefGoogle Scholar
  117. Wu EC, Zhang S, Hauser CA (2012) Self-assembling peptides as cell-interactive scaffolds. Adv Funct Mater 22:456–468CrossRefGoogle Scholar
  118. Wu Y, Zheng Q, Du J, Song Y, Wu B, Guo X (2006) Self-assembled IKVAV peptide nanofibers promote adherence of PC12 cells. J Huazhong Univ Sci Technol 26:594–596CrossRefGoogle Scholar
  119. Yamada M, Kadoya Y, Kasai S, Kato K, Mochizuki M, Nishi N, Watanabe N, Kleinman HK, Yamada Y, Nomizu M (2002) Ile-Lys-Val-ala-Val (IKVAV)-containing laminin α1 chain peptides form amyloid-like fibrils. FEBS Lett 530:48–52PubMedCrossRefGoogle Scholar
  120. Yang Y-H, Khan Z, Ma C, Lim HJ, Callahan LAS (2015) Optimization of adhesive conditions for neural differentiation of murine embryonic stem cells using hydrogels functionalized with continuous Ile-Lys-Val-ala-Val concentration gradients. Acta Biomater 21:55–62PubMedCrossRefGoogle Scholar
  121. Zhan X, Gao M, Jiang Y, Zhang W, Wong WM, Yuan Q, Su H, Kang X, Dai X, Zhang W (2013) Nanofiber scaffolds facilitate functional regeneration of peripheral nerve injury. Nanomedicine 9:305–315PubMedCrossRefGoogle Scholar
  122. Zhang P, Yin Y, Qiu T, Tao Y, Wang X (2014) Cytocompatibility evaluation of grafted IKVAV PLEOF hydrogels with bone marrow mesenchymal stem cells. J Wuhan Univ Technol-Mater Sci Ed 29:824–831CrossRefGoogle Scholar
  123. Zhang S (2003) Fabrication of novel biomaterials through molecular self-assembly. Nat Biotechnol 21:1171–1178PubMedCrossRefGoogle Scholar
  124. Zhang S, Gelain F, Zhao X (2005) Designer self-assembling peptide nanofiber scaffolds for 3D tissue cell cultures. Seminars in cancer biology, vol 15. Elsevier, Amsterdam, pp 413–420Google Scholar
  125. Zhang ZX, Zheng QX, Wu YC, Hao DJ (2010) Compatibility of neural stem cells with functionalized self-assembling peptide scaffold in vitro. Biotechnol Bioprocess Eng 15:545–551CrossRefGoogle Scholar
  126. Zheng Q, Wu Y, Guo X (2009) Two-dimensional effects of hydrogel self-organized from IKVAV-containing peptides on growth and differentiation of NSCs. J Wuhan Univ Technol-Mater Sci Ed 24:186–192CrossRefGoogle Scholar
  127. Zou Z, Zheng Q, Wu Y, Song Y, Wu B (2009) Growth of rat dorsal root ganglion neurons on a novel self-assembling scaffold containing IKVAV sequence. Mater Sci Eng C 29:2099–2103CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Sajad Sahab Negah
    • 1
    • 2
  • Alireza Khooei
    • 3
  • Fariborz Samini
    • 4
  • Ali Gorji
    • 1
    • 2
    • 5
    • 6
  1. 1.Department of Neuroscience, Faculty of MedicineMashhad University of Medical SciencesMashhadIran
  2. 2.Shefa Neuroscience Research CenterKhatam Alanbia HospitalTehranIran
  3. 3.Department of Pathology, Faculty of MedicineMashhad University of Medical SciencesMashhadIran
  4. 4.Department of Neurosurgery, Faculty of MedicineMashhad University of Medical SciencesMashhadIran
  5. 5.Department of Neurology and Department of NeurosurgeryWestfälische Wilhelms-Universität MünsterMünsterGermany
  6. 6.Epilepsy Research CenterWestfälische Wilhelms-Universität MünsterMünsterGermany

Personalised recommendations